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Two Expansin Genes, Atexpa4 and Atexpb5, Are Redundantly Required for Pollen Tube Growth and Atexpa4 Is Involved in Primary Root Elongation in Arabidopsis Thaliana

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Two Expansin Genes, Atexpa4 and Atexpb5, Are Redundantly Required for Pollen Tube Growth and Atexpa4 Is Involved in Primary Root Elongation in Arabidopsis Thaliana G C A T T A C G G C A T genes Article Two Expansin Genes, AtEXPA4 and AtEXPB5, Are Redundantly Required for Pollen Tube Growth and AtEXPA4 Is Involved in Primary Root Elongation in Arabidopsis thaliana Weimiao Liu 1,2, Liai Xu 1,2 , Hui Lin 3 and Jiashu Cao 1,2,4,* 1 Laboratory of Cell and Molecular Biology, Institute of Vegetable Science, Zhejiang University, Hangzhou 310058, China; [email protected] (W.L.); [email protected] (L.X.) 2 Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture, Hangzhou 310058, China 3 Crop Research Institute, Fujian Academy of Agricultural Sciences, Fuzhou 350013, China; [email protected] 4 Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Hangzhou 310058, China * Correspondence: [email protected]; Tel.: +86-131-8501-1958 Abstract: The growth of plant cells is inseparable from relaxation and expansion of cell walls. Expansins are a class of cell wall binding proteins, which play important roles in the relaxation of cell walls. Although there are many members in expansin gene family, the functions of most expansin genes in plant growth and development are still poorly understood. In this study, the functions of two expansin genes, AtEXPA4 and AtEXPB5 were characterized in Arabidopsis thaliana. AtEXPA4 and AtEXPB5 displayed consistent expression patterns in mature pollen grains and pollen tubes, but AtEXPA4 also showed a high expression level in primary roots. Two single mutants, atexpa4 and atexpb5, showed normal reproductive development, whereas atexpa4 atexpb5 double mutant was defective in pollen tube growth. Moreover, AtEXPA4 overexpression enhanced primary root Citation: Liu, W.; Xu, L.; Lin, H.; Cao, elongation, on the contrary, knocking out AtEXPA4 made the growth of primary root slower. Our J. Two Expansin Genes, AtEXPA4 and results indicated that AtEXPA4 and AtEXPB5 were redundantly involved in pollen tube growth and AtEXPB5, Are Redundantly Required AtEXPA4 was required for primary root elongation. for Pollen Tube Growth and AtEXPA4 Is Involved in Primary Root Keywords: Arabidopsis thaliana; expansin genes; AtEXPA4; AtEXPB5; pollen tube growth; root elongation Elongation in Arabidopsis thaliana. Genes 2021, 12, 249. https://doi.org/ 10.3390/genes12020249 1. Introduction Academic Editor: Christian Chevalier Plant growth and development are inseparable from cell proliferation and expansion. Received: 8 December 2020 Different from animal cells, plant cells are surrounded by cell walls, which are highly Accepted: 5 February 2021 Published: 10 February 2021 dynamic and complex networks [1]. Cells are always in a dynamic balance between the expansion of protoplasts and the restraint of cell walls, undergoing irreversible growth [2]. Publisher’s Note: MDPI stays neutral Although cell walls expand slowly while plants grow, some organs and tissues require with regard to jurisdictional claims in rapid expansion of cell walls during specific periods, such as fast-growing roots and published maps and institutional affil- pollen tubes. iations. Numerous cell wall synthesis and remodeling genes have been reported to be involved in cell wall expansion [3–9], including expansin genes. Expansins can weaken non-covalent bonds between cell wall polysaccharides, thereby promoting slippage and relaxation of cellulose microfibers, resulting in cell wall extension and cell expansion [10,11]. Expansins usually have two typical domains, DPBB_1 and Pollen_allerg_1, and most of expansins Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. have signal peptides [12]. DPBB_1 domain is often related to family-45 glycosyl hydro- This article is an open access article lase (GH45), and contains a conserved region that has the double-psi beta-barrel (DPBB) distributed under the terms and fold [13,14]. Although DPBB_1 is similar to GH45, expansins lack the β-1,4-glucanase ac- conditions of the Creative Commons tivity of GH45 enzymes, which in turn lacks the wall expanding activity of expansins [15]. Attribution (CC BY) license (https:// Pollen_allerg_1 is often a pollen allergen, which is found at the C-terminus of expansins [16]. creativecommons.org/licenses/by/ The expansin gene family with many members can be divided into two major subfamilies, 4.0/). namely EXPA and EXPB subfamilies [15]. The various temporal and spatial expression Genes 2021, 12, 249. https://doi.org/10.3390/genes12020249 https://www.mdpi.com/journal/genes Genes 2021, 12, 249 2 of 16 patterns of expansin genes imply that they perform corresponding functions in different developmental stages [12,17–19]. Many studies have shown that EXPA subfamily plays complex and diverse functions in plant growth and development. For example, Arabidop- sis thaliana EXPA2 (AtEXPA2) participates in seed germination under the regulation of upstream transcription factors [20–22]. AtEXPA5 participates in plant growth and develop- ment regulated by ethylene and brassinosteroids [23,24]. AtEXPA5 and Oryza sativa EXPA8 (OsEXPA8)[25,26] are both involved in the development of primary roots. The inhibition of their expressions reduces the length of primary root. Moreover, AtEXPA14 and AtEXPA17 participate in the growth of lateral roots and root hairs by the regulation of auxin-related transcription factor LBD18 [27,28]. However, researches on the roles of expansins in plant reproductive development are relatively limited. It was only confirmed that Zea mays EXPB1 (ZmEXPB1) showed a great influence on the growth of pollen tubes in vivo and positively affected the entry of pollens into ovules [29–31]. A previous study showed that two expansin genes, AtEXPA4 and AtEXPB5, were strongly expressed in dry pollen grains, imbibed pollen grains, and pollen tubes [32–36]. Here, we further confirmed the expression patterns of AtEXPA4 and AtEXPB5. By exploring phenotypes of mutants and overexpression lines, we found that AtEXPA4 and AtEXPB5 are redundantly involved in pollen tube elongation, and AtEXPA4 plays a positive role in primary root growth. 2. Materials and Methods 2.1. Plant Materials and Growth Conditions All transgenic plants used in this study were of Arabidopsis thaliana (A. thaliana) Columbia ecotype (Col-0) background and were obtained by Agrobacterium tumefaciens- mediated floral dip method [37]. The homozygous mutants atexpa4 and atexpb5 were obtained by CRISPR/Cas9 system [38]. Two off-target sites of AtEXPA4 and AtEXPB5 were predicted by the CRISPR-P 2.0 website (http://crispr.hzau.edu.cn/CRISPR2/ (accessed on 1 February 2020)), respectively. To obtain heterozygous double mutants of AtEXPA4 and AtEXPB5, atexpb5 and atexpa4 homozygous plants were used as female and male parents in a cross. The homozygous double mutants, atexpa4expb5, were generated by self-crossing with heterozygous F1 plants. The genotypes of 362 F2 plants were confirmed by PCR and sequencing, and genotype statistics and analysis were performed. A 1522-bp promoter sequence and the coding sequence of AtEXPA4 (splicing vari- ant: At2g39700.1) were amplified from Col-0 genomic DNA and inflorescence cDNA. A 1571-bp promoter sequence and the coding sequence of AtEXPB5 (splicing variant: At3g60570.1) were also amplified from Col-0 genomic DNA and inflorescence cDNA. Then they were subcloned into pBI101 vectors to create the fusion overexpression con- structs proAtEXPA4::EXPA4, proAtEXPB5::EXPB5 and the promoter analysis construct proAtEXPA4::GUS, proAtEXPB5::GUS. The complemented lines were obtained by trans- forming proAtEXPA4::EXPA4 and proAtEXPB5::EXPB5 into the double mutant atexpa4expb5, and named atexpa4expb5A4OE and atexpa4expb5B5OE, respectively. The homozygous overex- pression lines AtEXPA4OE, AtEXPB5OE and promoter analysis lines of AtEXPA4, AtEXPB5 −1 were identified from screening T3 plants on plates containing kanamycin (50 mg·L ). Two complementary lines were identified from screening T1 plants on plates containing kanamycin (50 mg·L−1). All seedlings were transplanted into soil, and grown in a 22 ◦C climate chamber under long-day conditions (16 h light/8 h dark). All the primers were listed in Table S1. For root phenotype analysis, the seeds of wild-type, atexpa4, atexpb5, AtEXPA4OE, and AtEXPB5OE were surface-sterilized with 75% ethanol for 5 min and washed 5 times with sterile water. Subsequently, these seeds were geminated on 1/2 Murashige and Skoog solid media and placed horizontally at 4 ◦C for 3 days. Next, plates were transferred to an artificial climate chamber and placed vertically on the platform, and then germinated at 22 ± 1 ◦C under 12 h light/12 h dark cycle. Genes 2021, 12, 249 3 of 16 2.2. mRNA Expression Analysis Trizol reagent (Invitrogen, Carlsbad, CA, USA) were used to extract total RNA from plant tissues and first-strand cDNA was synthesized by PrimerScript RT reagent Kit (TaKaRa, Kyoto, Japan) from 1 µg total RNA. The relative expression levels of corre- sponding genes in different tissues and organs were detected by quantitative real-time PCR (qRT-PCR), which were performed by using TaKaRa TB Green™ Premix Ex Taq™ II (Tli RNaseH Plus) on a Real-Time PCR machine (CFX96 Real-Time System, Bio-Rad, Carlsbad, CA, USA). Primers for AtEXPA4 and AtEXPB5 were listed in Supplemental Table S1. BETA-TUBULIN4 (At5g44340) was used as the reference gene for AtEXPA4 and AtEXPB5 expression in different tissues and different transgenic lines. All experiments were performed three biological replicates, and each biological replicate was performed three technical replicates. Moreover, transcript levels
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